Cloning and identification of tissue-specific expression of KCNN4 splice variants in rat colon

American Journal of Physiology - Cell Physiology

Volumn 299, Issue 2, 2010, Pages

  Barmeyer, Christian ^a   Rahner, Christoph ^a   Yang, Youshan ^a   Sigworth, Frederick J ^a   Binder, Henry J ^a   Rajendran, Vazhaikkurichi M ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apical membrane; Basolateral membrane; Epithelial cells; Potassium secretion; Smooth muscle

Indexed keywords

AMINO ACID; ANION; CALCIUM ACTIVATED POTASSIUM CHANNEL; COMPLEMENTARY DNA; GLUTAMINE; INTERMEDIATE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; INTERMEDIATE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL 4A; INTERMEDIATE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL 4B; INTERMEDIATE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL 4C; ISOPROTEIN; MEMBRANE PROTEIN; POTASSIUM CHANNEL; RUBIDIUM 86; UNCLASSIFIED DRUG; KCNN4 PROTEIN, RAT;

3' UNTRANSLATED REGION; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; BETA CHAIN; CELL MEMBRANE; COLON; COMPETITIVE INHIBITION; CONTROLLED STUDY; EPITHELIUM CELL; EXON; IMMUNOFLUORESCENCE; MALE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN MOTIF; RAT; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTH MUSCLE FIBER; AMINO ACID SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; BIOSYNTHESIS; COMPARATIVE STUDY; FEMALE; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; HUMAN; INTESTINE MUCOSA; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; SPRAGUE DAWLEY RAT; XENOPUS;

MAMMALIA; RATTUS;

AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; COLON; FEMALE; GENE EXPRESSION REGULATION; GENETIC VARIATION; HUMANS; INTERMEDIATE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; INTESTINAL MUCOSA; MALE; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; XENOPUS;

EID: 77955878802     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00091.2009     Document Type: Article

References (55)

1. Albaqumi M, Srivastava S, Li Z, Zhdnova O, Wulff H, Itani O, Wallace DP, Skolnik EY. KCa3.1.potassium channels are critical for cAMP-dependent chloride secretion and cyst growth in autosomal-dominant polycystic kidney disease. Kidney Int 74: 740-749, 2008.
2. Bakos E, Evers R, Szakacs G, Tusnady GE, Welker E, Szabo K., de Haas M, van Deemter L, Borst P, Varadi A, Sarkadi B. Functional multidrug resistance protein (MRP1) lacking the N-terminal transmembrane domain. J Biol Chem 273: 32167-32175, 1998.
3. Barrett KE, Keely SJ. Chloride secretion by the intestinal epithelium: molecular basis and regulatory aspects. Annu Rev Physiol 62: 535-572, 2000.
4. Begenisich T, Nakamoto T, Ovitt CE, Nehrke K, Brugnara C, Alper SL, and Melvin JE. Physiological roles of the intermediate conductance, Ca2+-activated potassium channel Kcnn4. J Biol Chem 279: 47681-47687, 2004.
5. Bernard K, Bogliolo S, Soriani O, Ehrenfeld J. Modulation of calcium-dependent chloride secretion by basolateral SK4-like channels in a human bronchial cell line. J Membr Biol 196: 15-31, 2003.
6. Biber J, Rechkemmer G, Bodmer M, Schroder P, Haase W, Murer H. Isolation of basolateral membranes from columnar cells of the proximal colon of the guinea pig. Biochim Biophys Acta 735: 1-11, 1983.
7. Bleich M, Riedemann N, Warth R, Kerstan D, Leipziger J, Hor M, Driessche WV, Greger R. Ca2+ regulated K+ and non-selective cation channels in the basolateral membrane of rat colonic crypt base cells. Pflügers Arch 432: 1011-1022, 1996.
8. Breitwieser GE. Mechanisms of K+ channel regulation. J Membr Biol 152: 1-11, 1996.
9. Chen MX, Gorman SA, Benson B, Singh K, Hieble JP, Michel MC, Tate SN, Trezise DJ. Small and intermediate conductance Ca(2+)-activated K+ channels confer distinctive patterns of distribution in human tissues and differential cellular localisation in the colon and corpus cavernosum. Naunyn Schmiedebergs Arch Pharmacol 369: 602-615, 2004.
10. Devor DC, Singh AK, Bridges RJ, Frizzell RA. Modulation of Cl-secretion by benzimidazolones. II. Coordinate regulation of apical GCl and basolateral GK. Am J Physiol Lung Cell Mol Physiol 271: L785-L795, 1996.
11. Fanger CM, Rauer H, Neben AL, Miller MJ, Wulff H, Rosa JC, Ganellin CR, Chandy KG, Cahalan MD. Calcium-activated potassium channels sustain calcium signaling in T lymphocytes. Selective blockers and manipulated channel expression levels. J Biol Chem 276: 12249-12256, 2001.
12. Fong P, Argent BE, Guggino WB, Gray MA. Characterization of vectorial chloride transport pathways in the human pancreatic duct adenocarcinoma cell line HPAF. Am J Physiol Cell Physiol 285: C433-C445, 2003.
13. Fordtran JS. Speculations on the pathogenesis of diarrhea. Fed Proc 26: 1405-1414, 1967.
14. Furness JB, Robbins HL, Selmer IS, Hunne B, Chen MX, Hicks GA, Moore S, Neylon CB. Expression of intermediate conductance potassium channel immunoreactivity in neurons and epithelial cells of the rat gastrointestinal tract. Cell Tissue Res 314: 179-189, 2003.
15. Gottardi CJ, Pietrini G, Roush DL, Caplan MJ. Sorting of ion transport proteins in polarized cells. J Cell Sci Suppl 17: 13-20, 1993.
16. Greger R, Bleich M, Warth R. New types of K+ channels in the colon. Wien Klin Wochenschr 109: 497-498, 1997.
17. Halm ST, Liao T, Halm DR. Distinct K+ conductive pathways are required for Cl- and K+ secretion across distal colonic epithelium. Am J Physiol Cell Physiol 291: C636-C648, 2006.
18. Hanley PJ, Musset B, Renigunta V, Limberg SH, Dalpke AH, Sus R, Heeg KM, Preisig-Muller R, Daut J. Extracellular ATP induces oscillations of intracellular Ca2+ and membrane potential and promotes transcription of IL-6 in macrophages. Proc Natl Acad Sci USA 101: 9479-9484, 2004.
19. Ishii TM, Silvia C, Hirschberg B, Bond CT, Adelman JP, Maylie J. A human intermediate conductance calcium-activated potassium channel. Proc Natl Acad Sci USA 94: 11651-11656, 1997.
20. + channel. Am J Physiol Cell Physiol 275: C848-C856, 1998.
21. + secretion through multiple KCa-type channels and regulation by IKCa channels in rat proximal colon. Am J Physiol Gastrointest Liver Physiol 285: G185-G196, 2003.
22. Joiner WJ, Wang LY, Tang MD, Kaczmarek LK. hSK4, a member of a novel subfamily of calcium-activated potassium channels. Proc Natl Acad Sci USA 94: 11013-11018, 1997.
23. Jung H. Topology and function of the Na+/proline transporter of Escherichia coli, a member of the Na+/solute cotransporter family. Biochim Biophys Acta 1365: 60-64, 1998.
24. Kast C, Canfield V, Levenson R, Gros P. Membrane topology of P-glycoprotein as determined by epitope insertion: transmembrane organization of the N-terminal domain of mdr3. Biochemistry 34: 4402-4411, 1995.
25. Kast C, Gros P. Topology mapping of the amino-terminal half of multidrug resistance-associated protein by epitope insertion and immuno-fluorescence. J Biol Chem 272: 26479-26487, 1997.
26. Kolski-Andreaco A, Tomita H, Shakkottai VG, Gutman GA, Cahalan MD, Gargus JJ, Chandy KG. SK3-1C, a dominant-negative suppressor of SKCa and IKCa channels. J Biol Chem 279: 6893-6904, 2004.
27. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580, 2001.
28. Lauf PK, Misri S, Chimote AA, Adragna NC. Apparent intermediate K conductance channel hyposmotic activation in human lens epithelial cells. Am J Physiol Cell Physiol 294: C820-C832, 2008.
29. Liou W, Geuze HJ, Slot JW. Improving structural integrity of cryosections for immunogold labeling. Histochem Cell Biol 106: 41-58, 1996.
30. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408, 2001.
31. Logsdon NJ, Kang J, Togo JA, Christian EP, Aiyar J. A novel gene, hKCa4, encodes the calcium-activated potassium channel in human T lymphocytes. J Biol Chem 272: 32723-32726, 1997.
32. Lomax RB, McNicholas CM, Lombes M, Sandle GI. Aldosterone-induced apical Na+ and K+ conductances are located predominantly in surface cells in rat distal colon. Am J Physiol Gastrointest Liver Physiol 266: G71-G82, 1994.
33. Meera P, Wallner M, Song M, Toro L. Large conductance voltage- and calcium-dependent K+ channel, a distinct member of voltage-dependent ion channels with seven N-terminal transmembrane segments (S0-S6), an extracellular N terminus, and an intracellular (S9-S10) C terminus. Proc Natl Acad Sci USA 94: 14066-14071, 1997.
34. Mense M, Rajendran V, Blostein R, Caplan MJ. Extracellular domains, transmembrane segments, and intracellular domains interact to determine the cation selectivity of Na,K- and gastric H,K-ATPase. Biochemistry 41: 9803-9812, 2002.
35. Muth TR, Caplan MJ. Transport protein trafficking in polarized cells. Annu Rev Cell Dev Biol 19: 333-366, 2003.
36. Neylon CB, Lang RJ, Fu Y, Bobik A, Reinhart PH. Molecular cloning and characterization of the intermediate-conductance Ca(2+)-activated K(+) channel in vascular smooth muscle: relationship between K(Ca) channel diversity and smooth muscle cell function. Circ Res 85: e33-43, 1999.
37. Nimigean CM, Magleby KL. Functional coupling of the beta(1) subunit to the large conductance Ca(2+)-activated K(+) channel in the absence of Ca(2+). Increased Ca(2+) sensitivity from a Ca(2+)-independent mechanism. J Gen Physiol 115: 719-736, 2000.
38. Rajendran VM, Kashgarian M, Binder HJ. Aldosterone induction of electrogenic sodium transport in the apical membrane vesicles of rat distal colon. J Biol Chem 264: 18638-18644, 1989.
39. Rajendran VM, Oesterlin M, Binder HJ. Sodium uptake across basolateral membrane of rat distal colon. Evidence for Na-H exchange and Na-anion cotransport. J Clin Invest 88: 1379-1385, 1991.
40. Reyes R, Duprat F, Lesage F, Fink M, Salinas M, Farman N, Lazdunski M. Cloning and expression of a novel pH-sensitive two pore domain K+ channel from human kidney. J Biol Chem 273: 30863-30869, 1998.
41. Rufo PA, Jiang L, Moe SJ, Brugnara C, Alper SL, Lencer WI. The antifungal antibiotic, clotrimazole, inhibits Cl- secretion by polarized monolayers of human colonic epithelial cells. J Clin Invest 98: 2066-2075, 1996.
42. Sandle GI, McNicholas CM, Lomax RB. Potassium channels in colonic crypts. Lancet 343: 23-25, 1994.
43. Sangan P, Kolla SS, Rajendran VM, Kashgarian M, Binder HJ. Colonic H-K-ATPase β-subunit: identification in apical membranes and regulation by dietary K depletion. Am J Physiol Cell Physiol 276: C350-C360, 1999.
44. Sangan P, Thevananther S, Sangan S, Rajendran VM, Binder HJ. Colonic H-K-ATPase α- and β-subunits express ouabain-insensitive H-KATPase. Am J Physiol Cell Physiol 278: C182-C189, 2000.
45. Sharma NR, Davis MJ. Mechanism of substance P-induced hyperpolarization of porcine coronary artery endothelial cells. Am J Physiol Heart Circ Physiol 266: H156-H164, 1994.
46. Shepherd MC, Duffy SM, Harris T, Cruse G, Schuliga M, Brightling CE, Neylon CB, Bradding P, Stewart AG. KCa3.1. Ca2+ activated K+ channels regulate human airway smooth muscle proliferation. Am J Respir Cell Mol Biol 37: 525-531, 2007.
47. Singh S, Syme CA, Singh AK, Devor DC, Bridges RJ. Benzimidazolone activators of chloride secretion: potential therapeutics for cystic fibrosis and chronic obstructive pulmonary disease. J Pharmacol Exp Ther 296: 600-611, 2001.
48. Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol 103: 755-766, 1986.
49. Stieger B, Marxer A, Hauri HP. Isolation of brush-border membranes from rat and rabbit colonocytes: is alkaline phosphatase a marker enzyme? J Membr Biol 91: 19-31, 1986.
50. 2+-activated potassium and volume-sensitive chloride channels in mouse mesenchymal stem cells. Am J Physiol Cell Physiol 295: C1409-C1416, 2008.
51. Toyama K, Wulff H, Chandy KG, Azam P, Raman G, Saito T, Fujiwara Y, Mattson DL, Das S, Melvin JE, Pratt PF, Hatoum OA, Gutterman DD, Harder DR, Miura H. The intermediate-conductance calcium-activated potassium channel KCa3.1 contributes to atherogenesis in mice and humans. J Clin Invest 118: 3025-3037, 2008.
52. Vandorpe DH, Shmukler BE, Jiang L, Lim B, Maylie J, Adelman JP, de Franceschi L, Cappellini MD, Brugnara C, Alper SL. cDNA cloning and functional characterization of the mouse Ca2+-gated K+ channel, mIK1. Roles in regulatory volume decrease and erythroid differentiation. J Biol Chem 273: 21542-21553, 1998.
53. Wang J, Morishima S, Okada Y. IK channels are involved in the regulatory volume decrease in human epithelial cells. Am J Physiol Cell Physiol 284: C77-C84, 2003.
54. Warth R, Hamm K, Bleich M, Kunzelmann K, von Hahn T, Schreiber R, Ullrich E, Mengel M, Trautmann N, Kindle P, Schwab A, Greger R. Molecular and functional characterization of the small Ca(2+)-regulated K+ channel (rSK4) of colonic crypts. Pflügers Arch 438: 437-444, 1999.
55. Wulff H, Miller MJ, Hansel W, Grissmer S, Cahalan MD, Chandy KG. Design of a potent and selective inhibitor of the intermediate-conductance Ca2+-activated K+ channel, IKCa1: a potential immunosuppressant. Proc Natl Acad Sci USA 97: 8151-8156, 2000.